Proteome analysis of the penicillin producer Penicillium chrysogenum: Characterization of protein changes during the industrial strain improvement

Molecular and Cellular Proteomics

Volumn 9, Issue 6, 2010, Pages 1182-1198

  Jami, Mohammad Saeid ^a   Barreiro, Carlos ^b   García Estrada, Carlos ^b   Martín, Juan Francisco ^a,b  

^a UNIVERSITY OF LEÓN   (Spain)

^b Institute of Biotechnology INBIOTEC Parque Científico de León   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANAZOLENE SODIUM; CARBON; CELLULOSE; CYSTEINE; ENZYME; ISOFLAVONOID; PENICILLIN G; PENTOSE PHOSPHATE; PIGMENT; PROTEOME; SORBITOL;

ARTICLE; BIOSYNTHESIS; CARBON SOURCE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ANALYSIS; FUNGAL STRAIN; FUNGAL VIRULENCE; GENOME; INDUSTRY; NONHUMAN; PENICILLIUM CHRYSOGENUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; STAINING; STRESS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS; WILD TYPE;

BIOSYNTHETIC PATHWAYS; BIOTECHNOLOGY; CARBOHYDRATE METABOLISM; CELL WALL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENERGY METABOLISM; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; INDUSTRY; INTRACELLULAR SPACE; OXIDATIVE STRESS; PENICILLINS; PENICILLIUM CHRYSOGENUM; PIGMENTATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEOME; PROTEOMICS; REFERENCE STANDARDS; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 77953172467     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900327-MCP200     Document Type: Article

References (69)

1. Liras, P., and Martín, J. F. (2009) β-Lactam antibiotics, in Encyclopedia of Microbiology (Schaechter, M., ed) 3rd Ed., pp. 274-289, Elsevier Ltd., Oxford
2. García-Rico, R. O., Fierro, F., Mauriz, E., Gómez, A., Fernández-Bodega, M. A., and Martín, J. F. (2008) The heterotrimeric Gα protein Pga1 regulates biosynthesis of penicillin, chrysogenin and roquefortine in Penicillium chrysogenum. Microbiology 154, 3567-3578
3. Fleming, A. (1929) On the antibacterial action of cultures of a penicillium with special reference to their use in the isolation of B. influenza. Br. J. Exp. Pathol. 10, 226-236
4. Raper, K. B., Alexander, D. F., and Coghill, R. D. (1944) Penicillin. II. Natural variation and penicillin production in Penicillium notatum and allied species. J. Bacteriol. 48, 639-659
5. Elander, R. P. (1983) Strain improvement and preservation of beta-lactam producing microorganisms, in Antibiotics Containing the Beta-lactam Structure I (Demain, A. L., and Solomon, N., eds) pp. 97-146, Springer-Verlag, New York
6. Elander, R. P. (2002) University of Wisconsin contributions to the early development of penicillin and cephalosporin antibiotics. SIM News 52, 270-278
7. Demain, A. L., and Elander, R. P. (1999) The β-lactam antibiotics: past, present and future. Antonie Leeuwenhoek 75, 5-19
8. Lein, J. (1986) The Panlabs Penicillium strain improvement program, in Overproduction of Microbial Metabolites (Vanek, Z., and Hostalek, Z., eds) pp. 105-140, Butterworths, Stoneham, MA
9. Gouka, R. J., van Hartingsveldt, W., Bovenberg R. A., van den Hondel, C. A., and van Gorcom, R. F. (1991) Cloning of a nitrate-nitrite reductase gene cluster of Penicillium chrysogenum and use of the niaD gene as a homologous marker. J. Biotechnol. 20, 189-199
10. Fierro, F., Barredo, J. L., Díez, B., Gutierrez, S., Fernández, F. J., and Martín, J. F. (1995) The penicillin gene cluster is amplified in tandem repeats linked by conserved hexanucleotide sequences. Proc. Natl. Acad. Sci. U.S.A. 92, 6200-6204
11. Rodríguez-Sáiz, M., Barredo, J. L., Moreno, M. A., Fernández-Cañón, J. M., Peñalva, M. A., and Díez, B. (2001) Reduced function of a phenylacetateoxidizing cytochrome P450 caused strong genetic improvement in early phylogeny of penicillin-producing strains. J. Bacteriol. 183, 5465-5471
12. Newbert, R. W., Barton, B., Greaves, P., Harper, J., and Turner, G. (1997) Analysis of a commercially improved Penicillium chrysogenum strain series: involvement of recombinogenic regions in amplification and deletion of the penicillin biosynthesis gene cluster. J. Ind. Microbiol. Biotechnol. 19, 18-27 (Pubitemid 27467128)
13. Fierro, F., García-Estrada, C., Castillo, N. I., Rodríguez, R., Velasco-Conde, T., and Martín, J. F. (2006) Transcriptional and bioinformatic analysis of the 56.8 kb DNA region amplified in tandem repeats containing the penicillin gene cluster in Penicillium chrysogenum. Fungal Genet. Biol. 43, 618-629 (Pubitemid 44175874)
14. Müller, W. H., van der Krift, T. P., Krouwer, A. J., Wösten, H. A., van der Voort, L. H., Smaal, E. B., and Verkleij, A. J. (1991) Localization of the pathway of the penicillin biosynthesis in Penicillium chrysogenum. EMBO J. 10, 489-495
15. Lamas-Maceiras, M., Vaca, I., Rodríguez, E., Casqueiro, J., and Martín, J. F. (2006) Amplification and disruption of the phenylacetyl-CoA ligase gene of Penicillium chrysogenum encoding an aryl-capping enzyme that supplies phenylacetic acid to the isopenicillin N-acyltransferase. Biochem. J. 395, 147-155
16. Martín, J. F., Ullán, R. V., and García-Estrada, C. (2010) Regulation and compartmentalization of β-lactam biosynthesis. Microb. Biotechnol., 3, 285-299
17. van den Berg, M. A., Albang, R., Albermann, K., Badger, J. H., Daran, J. M., Driessen, A. J., Garcia-Estrada, C., Fedorova, N. D., Harris, D. M., Heijne, W. H., Joardar, V., Kiel, J. A., Kovalchuk, A., Martín, J. F., Nierman, W. C., Nijland, J. G., Pronk, J. T., Roubos, J. A., van der Klei, I. J., van Peij, N. N., Veenhuis, M., von Döhren, H., Wagner, C., Wortman, J., and Bovenberg, R. A. (2008) Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 26, 1161-1168
18. Hwang, K. H., Carapito, C., Böhmer, S., Leize, E., Van Dorsselaer, A., and Bernhardt, R. (2006) Proteome analysis of Schizosaccharomyces pombe by two-dimensional gel electrophoresis and mass spectrometry. Proteomics 6, 4115-4129
19. Melin, P., Schnürer, J., and Wagner, E. G. (2002) Proteome analysis of Aspergillus nidulans reveals proteins associated with the response to the antibiotic concanamycin A, produced by Streptomyces species. Mol. Genet. Genomics 267, 695-702 (Pubitemid 35013676)
20. Kniemeyer, O., Lessing, F., Scheibner, O., Hertweck, C., and Brakhage, A. A. (2006) Optimisation of a 2-D gel electrophoresis protocol for the human pathogenic fungus Aspergillus fumigatus. Curr. Genet. 49, 178-189
21. Vödisch, M., Albrecht, D., Lessing, F, Schmidt, A. D., Winkler, R., Guthke, R., Brakhage, A. A., and Kniemeyer, O. (2009) Two-dimensional proteome reference maps for the human pathogenic filamentous fungus Aspergillus fumigatus. Proteomics 9, 1407-1415
22. Shevchenko, A., Jensen, O. N., Podtelejnikov, A. V., Sagliocco, F., Wilm, M., Vorm, O., Mortensen, P., Shevchenko, A., Boucherie, H., and Mann, M. (1996) Linking genome and proteome by mass spectrometry: largescale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. U.S.A. 93, 14440-14445 (Pubitemid 26418985)
23. Bruckmann, A., Hensbergen, P. J., Balog, C. I., Deelder, A. M., Brandt, R., Snoek, I. S., Steensma, H. Y., and van Heusden, G. P. (2009) Proteome analysis of aerobically and anaerobically grown Saccharomyces cerevisiae cells. J. Proteomics 71, 662-669
24. Kiel, J. A., van den Berg, M. A., Fusetti, F., Poolman, B., Bovenberg, R. A., Veenhuis, M., and van der Klei, I. J. (2009) Matching the proteome to the genome: the microbody of penicillin-producing Penicillium chrysogenum cells. Funct. Integr. Genomics 9, 167-184
25. Casqueiro, J., Bañuelos, O., Gutiérrez, S., Hijarrubia, M. J., and Martín, J. F. (1999) Intrachromosomal recombination between direct repeats in Penicillium chrysogenum: gene conversion and deletion events. Mol. Gen. Genet. 261, 994-1000 (Pubitemid 29397048)
26. Kosalková, K., García-Estrada, C., Ullán, R. V., Godio, R. P., Feltrer, R., Teijeira, F., Mauriz, E., and Martín, J. F. (2009) The global regulator LaeA controls penicillin biosynthesis, pigmentation and sporulation, but not roquefortine C synthesis in Penicillium chrysogenum. Biochimie 91, 214-225
27. Fernández-Acero, F. J., Jorge, I., Calvo, E., Vallejo, I., Carbú, M., Camafeita, E., López, J. A., Cantoral, J. M., and Jorrín, J. (2006) Two-dimensional electrophoresis protein profile of the phytopathogenic fungus Botrytis cinerea. Proteomics 6, S88-S96
28. Candiano, G., Bruschi, M., Musante, L., Santucci, L., Ghiggeri, G. M., Carnemolla, B., Orecchia, P., Zardi, L., and Righetti, P. G. (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25, 1327-1333 (Pubitemid 38801651)
29. Havlis, J., Thomas, H., Sebela, M., and Shevchenko, A. (2003) Fast-response proteomics by accelerated in-gel digestion of proteins. Anal. Chem. 75, 1300-1306 (Pubitemid 36397161)
30. Díez, B., Schleissner, C., Moreno, M. A., Rodríguez, M., Collados, A., and Barredo, J. L. (1998) The manganese superoxide dismutase from the penicillin producer Penicillium chrysogenum. Curr. Genet. 33, 387-394
31. Ruepp, A., Zollner, A., Maier, D., Albermann, K., Hani, J., Mokrejs, M., Tetko, I., Güldener, U., Mannhaupt, G., Münsterkötter, M., and Mewes, H. W. (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 32, 5539-5545 (Pubitemid 39545671)
32. C103S of the isopenicillin N acyltransferase is transported inside peroxisomes and regulates its self-processing. Fungal Genet. Biol. 45, 1043-1052
33. Kovacevic, S., Tobin, M. B., and Miller, J. R. (1990) The beta-lactam biosynthesis genes for isopenicillin N epimerase and deacetoxycephalosporin C synthetase are expressed from a single transcript in Streptomyces clavuligerus. J. Bacteriol. 172, 3952-3958 (Pubitemid 20213379)
34. Coque, J. J., Enguita, F. J., Martín, J. F., and Liras, P. (1995) A two-protein component 7 alpha-cephem-methoxylase encoded by two genes of the cephamycin C cluster converts cephalosporin C to 7-methoxycephalosporin C. J. Bacteriol. 177, 2230-2235
35. Kennedy, J., Auclair, K., Kendrew, S. G., Park, C., Vederas, J. C., and Hutchinson, C. R. (1999) Modulation of polyketide synthase activity by accessory proteins during lovastatin biosynthesis. Science 284, 1368-1372 (Pubitemid 29289665)
36. Parsons, J. F., Calabrese, K., Eisenstein, E., and Ladner, J. E. (2004) Structure of the phenazine biosynthesis enzyme PhzG. Acta Crystallogr. D Biol. Crystallogr. 60, 2110-2113 (Pubitemid 41087566)
37. Ehrlich, K. C., Yu J., and Cotty, P. J. (2005) Aflatoxin biosynthesis gene clusters and flanking regions. J. Appl. Microbiol. 99, 518-527 (Pubitemid 41215829)
38. Keller, N. P., Kantz, N. J., and Adams, T. H. (1994) Aspergillus nidulans verA is required for production of the mycotoxin sterigmatocystin. Appl. Environ. Microbiol. 60, 1444-1450
39. Keller, N. P., Segner, S., Bhatnagar, D., and Adams, T. H. (1995) stcS, a putative P-450 monooxygenase, is required for the conversion of versicolorin A to sterigmatocystin in Aspergillus nidulans. Appl. Environ. Microbiol. 61, 3628-3632
40. Dixon, R. A., and Steele, C. L. (1999) Flavonoids and isoflavonoids - a gold mine for metabolic engineering. Trends Plant Sci. 4, 394-400 (Pubitemid 129751364)
41. Kawaguchi, T., Enoki, T., Tsurumaki, S., Sumitani, J., Ueda, M., Ooi, T., and Arai, M. (1996) Cloning and sequencing of the cDNA encoding beta-glucosidase 1 from Aspergillus aculeatus. Gene 173, 287-288 (Pubitemid 26302478)
42. Costenoble, R., Valadi, H., Gustafsson, L., Niklasson, C., and Franzén, C. J. (2000) Microaerobic glycerol formation in Saccharomyces cerevisiae. Yeast 16, 1483-1495
43. Goodwin, G. W., Rougraff, P. M., Davis, E. J., and Harris, R. A. (1989) Purification and characterization of methylmalonate-semialdehyde dehydrogenase from rat liver. Identity to malonate-semialdehyde dehydrogenase. J. Biol. Chem. 264, 14965-14971 (Pubitemid 19237325)
44. Zhang, Y. X., Tang, L., and Hutchinson, C. R. (1996) Cloning and characterization of a gene (msdA) encoding methylmalonic acid semialdehyde dehydrogenase from Streptomyces coelicolor. J. Bacteriol. 178, 490-495 (Pubitemid 26030604)
45. Gómez, B. L., and Nosanchuk, J. D. (2003) Melanin and fungi. Curr. Opin. Infect. Dis. 16, 91-96
46. Hadas, Y., Goldberg, I., Pines, O., and Prusky, D. (2007) Involvement of gluconic acid and glucose oxidase in the pathogenicity of Penicillium expansum in apples. Phytopathology 97, 384-390 (Pubitemid 46348962)
47. Hwang, C. S., Flaishman, M. A., and Kolattukudy, P. E. (1995) Cloning of a gene expressed during appressorium formation by Colletotrichum gloeosporioides and a marked decrease in virulence by disruption of this gene. Plant Cell 7, 183-193
48. Beauvais, A., Monod, M., Debeaupuis, J. P., Diaquin, M., Kobayashi, H., and Latgé, J. P. (1997) Biochemical and antigenic characterization of a new dipeptidyl-peptidase isolated from Aspergillus fumigatus. J. Biol. Chem. 272, 6238-6244
49. Harris, D. M., van der Krogt, Z. A., van Gulik, W. M., van Dijken, J. P., and Pronk, J. T. (2007) Formate as an auxiliary substrate for glucose-limited cultivation of Penicillium chrysogenum: impact on penicillin G production and biomass yield. Appl. Environ. Microbiol. 73, 5020-5025
50. Kosalková, K., Marcos, A. T., and Martín, J. F. (2001) A moderate amplification of the mecB gene encoding cystathionine-γ-lyase stimulates cephalosporin biosynthesis in Acremonium chrysogenum. J. Ind. Microbiol. Biotechnol. 27, 252-258
51. Schoondermark-Stolk, S. A., Tabernero, M., Chapman, J., Ter Schure, E. G., Verrips, C. T., Verkleij, A. J., and Boonstra J. (2005) Bat2p is essential in Saccharomyces cerevisiae for fusel alcohol production on the non-fermentable carbon source ethanol. FEMS Yeast Res. 5, 757-766 (Pubitemid 40558923)
52. Nosaka, K., Nishimura, H., Kawasaki, Y., Tsujihara, T., and Iwashima, A. (1994) Isolation and characterization of the THI6 gene encoding a bifunctional thiamin-phosphate pyrophosphorylase/hydroxyethylthiazole kinase from Saccharomyces cerevisiae. J. Biol. Chem. 269, 30510-30516 (Pubitemid 24376533)
53. Mizote, T., Tsuda, M., Smith, D. D., Nakayama, H., and Nakazawa, T. (1999) Cloning and characterization of the thiD/J gene of Escherichia coli encoding a thiamin-synthesizing bifunctional enzyme, hydroxymethylpyrimidine kinase/phosphomethylpyrimidine kinase. Microbiology 145, 495-501 (Pubitemid 29090104)
54. Moiseeva, O. V., Solyanikova, I. P., Kaschabek, S. R., Gröning, J., Thiel, M., Golovleva, L. A., and Schlömann, M. (2002) A new modified ortho cleavage pathway of 3-chlorocatechol degradation by Rhodococcus opacus 1CP: genetic and biochemical evidence. J. Bacteriol. 184, 5282-5292
55. Dixon, R. A. (2001) Natural products and disease resistance. Nature 411, 843-847
56. Bakker, H., Kleczka, B., Gerardy-Schahn, R., and Routier, F. H. (2005) Identification and partial characterization of two eukaryotic UDP-galactopyranose mutases. Biol. Chem. 386, 657-661 (Pubitemid 41460263)
57. Beverley, S. M., Owens, K. L., Showalter, M., Griffith, C. L., Doering, T. L., Jones, V. C., and McNeil, M. R. (2005) Eukaryotic UDP-galactopyranose mutase (GLF gene) in microbial and metazoal pathogens. Eukaryot. Cell 4, 1147-1154
58. Kelly, J. M., Drysdale, M. R., Sealy-Lewis, H. M., Jones, I. G., and Lockington, R. A. (1990) Alcohol dehydrogenase III in Aspergillus nidulans is anaerobically induced and post-transcriptionally regulated. Mol. Gen. Genet. 222, 323-328
59. Kawasaki, N., Sugatani, J., and Saito, K. (1975) Studies on a phospholipase B from Penicillium notatum. Purification, properties, and mode of action. J. Biochem. 77, 1233-1244
60. Whiteman, P. A., Abraham, E. P., Baldwin, J. E., Fleming, M. D., Schofield, C. J., Sutherland, J. D., and Willis, A. C. (1990) Acyl coenzyme A: 6-aminopenicillanic acid acyltransferase from Penicillium chrysogenum and Aspergillus nidulans. FEBS Lett. 262, 342-344
61. Tobin, M. B., Baldwin, J. E., Cole, S. C., Miller, J. R., Skatrud, P. L., and Sutherland, J. D. (1993) The requirement for subunit interaction in the production of Penicillium chrysogenum acyl-coenzyme A: isopenicillin N acyltransferase in Escherichia coli. Gene 132, 199-206 (Pubitemid 23314635)
62. Nasution, U., van Gulik, W. M., Ras, C., Proell, A., and Heijnen, J. J. (2008) A metabolome study of the steady-state relation between central metabolism, amino acid biosynthesis and penicillin production in Penicillium chrysogenum. Metab. Eng. 10, 10-23 (Pubitemid 350298909)
63. Kosalková, K., Rodríguez-Sáiz, M., Barredo, J. L., and Martín, J. F. (2007) Binding of the PTA1 transcriptional activator to the divergent promoter region of the first two genes of the penicillin pathway in different Penicillium species. Curr. Genet. 52, 229-237
64. Shreve, D. S., Holloway, M. P., Haggerty, J. C., 3rd, and Sable, H. Z. (1983) The catalytic mechanism of transketolase. Thiamin pyrophosphate-derived transition states for transketolase and pyruvate dehydrogenase are not identical. J. Biol. Chem. 258, 12405-12408
65. Jørgensen, H., Nielsen, J., Villadsen, J., and Møllgaard, H. (1995) Metabolic flux distributions in Penicillium chrysogenum during fed-batch cultivations. Biotechnol. Bioeng. 46, 117-131
66. Henriksen, C. M., Christensen, L. H., Nielsen, J., and Villadsen, J. (1996) Growth energetics and metabolic fluxes in continuous cultures of Penicillium chrysogenum. J. Biotechnol. 45, 149-164
67. van Gulik, W. M., de Laat, W. T., Vinke, J. L., and Heijnen, J. J. (2000) Application of metabolic flux analysis for the identification of metabolic bottlenecks in the biosynthesis of penicillin-G. Biotechnol. Bioeng. 68, 602-618
68. Kleijn, R. J., Liu, F., van Winden, W. A., van Gulik, W. M., Ras, C., and Heijnen, J. J. (2007) Cytosolic NADPH metabolism in penicillin-G producing and non-producing chemostat cultures of Penicillium chrysogenum. Metab. Eng. 9, 112-123
69. Harris, D. M., Westerlaken, I., Schipper, D., van der Krogt, Z. A., Gombert, A. K., Sutherland, J., Raamsdonk, L. M., van den Berg, M. A., Bovenberg, R. A., Pronk, J. T., and Daran, J. M. (2009) Engineering of Penicillium chrysogenum for fermentative production of a novel carbamoylated cephem antibiotic precursor. Metab. Eng. 11, 125-137